Phosphorus nutrition strategies in a symbiodiniacean species: Implications in coral-alga symbiosis facing increasing phosphorus deficiency in future warmer oceans

Coral reefs thrive in the oligotrophic ocean and rely on symbiotic algae
to acquire nutrients. Global warming is projected to intensify
surface ocean nutrient deficiency and anthropogenic discharge of wastes
with high nitrogen (N): phosphorus (P) ratios can exacerbate P nutrient
limitation. However, our understanding on how symbiotic algae cope with P
deficiency is limited. Here, we investigated the responses of a coral
symbiotic species of Symbiodiniaceae, Cladocopium goreaui, to
P-limitation by examining its physiological performance and transcriptomic
profile. Under P stress, C. goreaui exhibited decreases in algal
growth, photosynthetic efficiency, and cellular P content but enhancement
in carbon fixation, N assimilation, N:P ratio, and energy metabolism, with
downregulated expression of carbohydrate exporter genes. Besides, C.
goreaui showed flexible mechanisms of utilizing different dissolved
organic phosphorus to relieve P deficiency. When provided glycerol
phosphate, C. goreaui hydrolyzed it extracellularly to produce phosphate
for uptake. When grown on phytate, in contrast, C. goreaui upregulated the
endocytosis pathway while no dissolved inorganic phosphorus was released
into the medium, suggesting that phytate was transported into the cell,
potentially via the endocytosis pathway. This study sheds light on the
survival strategies of C. goreaui and potential weakening of its
role as an organic carbon supplier in P-limited environments, underscoring
the importance of more systematic investigation on future projections of
such effects.